Ecology of Endozoicomonadaceae in three coral genera across the Pacific Ocean

Abstract

Health and resilience of the coral holobiont depend on diverse bacterial communities often dominated by key marine symbionts of the Endozoicomonadaceae family. The factors controlling their distribution and their functional diversity remain, however, poorly known. Here, we study the ecology of Endozoicomonadaceae at an ocean basin-scale by sampling specimens from three coral genera (Pocillopora, Porites, Millepora) on 99 reefs from 32 islands across the Pacific Ocean. The analysis of 2447 metabarcoding and 270 metagenomic samples reveals that each coral genus harbored a distinct new species of Endozoicomonadaceae. These species are composed of nine lineages that have distinct biogeographic patterns. The most common one, found in Pocillopora, appears to be a globally distributed symbiont with distinct metabolic capabilities, including the synthesis of amino acids and vitamins not produced by the host. The other lineages are structured partly by the host genetic lineage in Pocillopora and mainly by the geographic location in Porites. Millepora is more rarely associated to Endozoicomonadaceae. Our results show that different coral genera exhibit distinct strategies of host-Endozoicomonadaceae associations that are defined at the bacteria lineage level.

A novel, tissue-associated and vertically transmitted bacterial symbiont in the coralPocillopora acuta

“…S6) revealed Pac_P3-11-1 encodes several genes indicative of host-symbiont interactions, including type II and type III secretion systems, 35 eukaryotic-like proteins (Table S7), and three secondary metabolites with putative antimicrobial activity (Table S8). This gene repertoire is similar to that of other coral-associated Endozoicomonadaceae [3,4,[8][9][10] and may regulate host colonization, aggregation, and vertical transmission. Additionally, we recovered pathways for the biosynthesis of all amino acids (except phenylalanine, tyrosine, and arginine), as well as riboflavin (vitamin B2), pantothenate (B5), pyridoxin (B6), biotin (B7), and folate (B9), which could assist with coral metabolism [3,4,9,10,16].…”

“…This gene repertoire is similar to that of other coral-associated Endozoicomonadaceae [3,4,[8][9][10] and may regulate host colonization, aggregation, and vertical transmission. Additionally, we recovered pathways for the biosynthesis of all amino acids (except phenylalanine, tyrosine, and arginine), as well as riboflavin (vitamin B2), pantothenate (B5), pyridoxin (B6), biotin (B7), and folate (B9), which could assist with coral metabolism [3,4,9,10,16]. Finally, Pac_P3-11-1 shows potential for the scavenging of reactive oxygen species, which are believed to drive coral bleaching when present in excess [17], as it possesses pathways for the synthesis of the antioxidants heme, lipoic acid, and glutathione, and the dsyB gene, essential for the synthesis of dimethylsulfonioproprionate [18].…”

“…However, the identification and characterization of CAMA-forming bacteria in corals remains in its infancy. The most common CAMA bacteria belong to the Endozoicomonas genus [3,4,7], widespread coral symbionts generally considered to be mutualistic through sulfur cycling and B vitamin synthesis [3,[7][8][9][10]. Simkania sp.…”

Microbiome ecological memory and responses to repeated marine heatwaves clarify variation in coral bleaching and mortality

“…For example, multiple strains of the proposed mutualist Endozoicomonadaceae have been observed in Pocillopora spp. in Mo'orea, and strain‐level differences of this family may affect microbiome trajectories during disturbance (Hochart et al., 2023). In A. retusa and Pocillopora spp., patterns in alpha and beta diversity in response to heat stress directly mirror Endozoicomonadaceae relative abundance, in that elevated alpha diversity, beta dissimilarity, and beta dispersion are associated with a decline in Endozoicomonadaceae relative abundance, which is a pattern previously observed (Maher et al., 2020; Neave et al., 2016; Ziegler et al., 2019).…”

Unlocking the genomic potential of Red Sea coral probiotics

“…Vitamin B12 is involved in several metabolic pathways, including the production of the antioxidants glutathione and DMSP 102 , which are important for neutralizing high concentrations of ROS generated from heat stress events 33,43 . Bacteria that exist in association with corals possess genes encoding for proteins related to the biosynthesis of essential vitamins, such as B1, B2, and B7, whereas their coral host does not have the capacity to produce them 103 . This suggests that the coral holobiont can only take up these essential vitamins through heterotrophic feeding and/or from its bacterial symbionts.…”